Disruption of Rolandic Gamma-Band Functional Connectivity by Seizures is Associated with Motor Impairments in Children with Epilepsy

Division of Neurosurgery, Hospital for Sick Children, Toronto, Ontario, Canada.
PLoS ONE (Impact Factor: 3.23). 06/2012; 7(6):e39326. DOI: 10.1371/journal.pone.0039326
Source: PubMed


Although children with epilepsy exhibit numerous neurological and cognitive deficits, the mechanisms underlying these impairments remain unclear. Synchronization of oscillatory neural activity in the gamma frequency range (>30 Hz) is purported to be a mechanism mediating functional integration within neuronal networks supporting cognition, perception and action. Here, we tested the hypothesis that seizure-induced alterations in gamma synchronization are associated with functional deficits. By calculating synchrony among electrodes and performing graph theoretical analysis, we assessed functional connectivity and local network structure of the hand motor area of children with focal epilepsy from intracranial electroencephalographic recordings. A local decrease in inter-electrode phase synchrony in the gamma bands during ictal periods, relative to interictal periods, within the motor cortex was strongly associated with clinical motor weakness. Gamma-band ictal desychronization was a stronger predictor of deficits than the presence of the seizure-onset zone or lesion within the motor cortex. There was a positive correlation between the magnitude of ictal desychronization and impairment of motor dexterity in the contralateral, but not ipsilateral hand. There was no association between ictal desynchronization within the hand motor area and non-motor deficits. This study uniquely demonstrates that seizure-induced disturbances in cortical functional connectivity are associated with network-specific neurological deficits.

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    • "One putative mechanism involves interictal discharges, which have been shown to suspend DMN activity in previous studies evaluating adults with epilepsy [Gotman et al., 2005]. Ictal dynamics have also been previously shown to disrupt synchronization of neural oscillations in eloquent brain regions that may be distant from site of seizure origin [Ibrahim et al., 2012]. Such disruptions have been associated with specific clinical deficits that persist beyond the ictal period. "
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    • "Individual differences in neuronal oscillations have also been related to the emergence of perceptual abilities (Csisbra et al., 2000) and the development of cognitive abilities (Benasich et al., 2008; Gou et al., 2011). Atypical oscillatory synchronization in brain networks has been related also to functional impairments and cognitive difficulties in other pediatric populations (Doesburg et al., 2011; Ibrahim et al., 2012). These age-dependent changes are understood to reflect changes in the architecture of functional brain networks, reflecting maturation in pathways of information flow in the brain (Boersma et al., 2011, 2013a). "
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